TRPV1 Channels Mediate Long-Term Depression at Synapses on Hippocampal Interneurons

Neuron

Volumn 57, Issue 5, 2008, Pages 746-759

  Gibson, Helen E ^a   Edwards, Jeffrey G ^a   Page, Rachel S ^a   Van Hook, Matthew J ^a   Kauer, Julie A ^a  

^a BROWN UNIVERSITY   (United States)

Author keywords

MOLNEURO

Indexed keywords

12 HYDROXYICOSATETRAENOIC ACID; CAPSAICIN; ICOSANOID; VANILLOID RECEPTOR 1;

ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; HIPPOCAMPUS; INTERNEURON; LONG TERM DEPRESSION; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SYNAPSE;

ANIMALS; HIPPOCAMPUS; INTERNEURONS; LONG-TERM SYNAPTIC DEPRESSION; MICE; MICE, INBRED C57BL; MICE, MUTANT STRAINS; ORGAN CULTURE TECHNIQUES; RATS; RATS, SPRAGUE-DAWLEY; SYNAPSES; TRPV CATION CHANNELS;

EID: 40249111593     PISSN: 08966273     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuron.2007.12.027     Document Type: Article

References (74)

1. Al-Hayani A., Wease K.N., Ross R.A., Pertwee R.G., and Davies S.N. The endogenous cannabinoid anandamide activates vanilloid receptors in the rat hippocampal slice. Neuropharmacology 41 (2001) 1000-1005
2. Benham C.D., Gunthorpe M.J., and Davis J.B. TRPV channels as temperature sensors. Cell Calcium 33 (2003) 479-487
3. Caterina M.J., Schumacher M.A., Tominaga M., Rosen T.A., Levine J.D., and Julius D. The capsaicin receptor: a heat-activated ion channel in the pain pathway. Nature 389 (1997) 816-824
4. Caterina M.J., Leffler A., Malmberg A.B., Martin W.J., Trafton J., Petersen-Zeitz K.R., Koltzenburg M., Basbaum A.I., and Julius D. Impaired nociception and pain sensation in mice lacking the capsaicin receptor. Science 288 (2000) 306-313
5. Chen K., Neu A., Howard A.L., Foldy C., Echegoyen J., Hilgenberg L., Smith M., Mackie K., and Soltesz I. Prevention of plasticity of endocannabinoid signaling inhibits persistent limbic hyperexcitability caused by developmental seizures. J. Neurosci. 27 (2007) 46-58
6. Chevaleyre V., and Castillo P.E. Heterosynaptic LTD of hippocampal GABAergic synapses: a novel role of endocannabinoids in regulating excitability. Neuron 38 (2003) 461-472
7. Chevaleyre V., and Castillo P.E. Endocannabinoid-mediated metaplasticity in the hippocampus. Neuron 43 (2004) 871-881
8. Chevaleyre V., Takahashi K.A., and Castillo P.E. Endocannabinoid-mediated synaptic plasticity in the CNS. Annu. Rev. Neurosci. 29 (2006) 37-76
9. Cristino L., de Petrocellis L., Pryce G., Baker D., Guglielmotti V., and Di Marzo V. Immunohistochemical localization of cannabinoid type 1 and vanilloid transient receptor potential vanilloid type 1 receptors in the mouse brain. Neuroscience 139 (2006) 1405-1415
10. Cui M., Honore P., Zhong C., Gauvin D., Mikusa J., Hernandez G., Chandran P., Gomtsyan A., Brown B., Bayburt E.K., et al. TRPV1 receptors in the CNS play a key role in broad-spectrum analgesia of TRPV1 antagonists. J. Neurosci. 26 (2006) 9385-9393
11. del Castillo J., and Katz B. Quantal components of the end-plate potential. J. Physiol. 124 (1954) 560-573
12. De Petrocellis L., and Di Marzo V. Lipids as regulators of the activity of transient receptor potential type V1 (TRPV1) channels. Life Sci. 77 (2005) 1651-1666
13. De Petrocellis L., Bisogno T., Maccarrone M., Davis J.B., Finazzi-Agro A., and Di Marzo V. The activity of anandamide at vanilloid VR1 receptors requires facilitated transport across the cell membrane and is limited by intracellular metabolism. J. Biol. Chem. 276 (2001) 12856-12863
14. Doly S., Fischer J., Salio C., and Conrath M. The vanilloid receptor-1 is expressed in rat spinal dorsal horn astrocytes. Neurosci. Lett. 357 (2004) 123-126
15. Feinmark S.J., Begum R., Tsvetkov E., Goussakov I., Funk C.D., Siegelbaum S.A., and Bolshakov V.Y. 12-lipoxygenase metabolites of arachidonic acid mediate metabotropic glutamate receptor-dependent long-term depression at hippocampal CA3-CA1 synapses. J. Neurosci. 23 (2003) 11427-11435
16. Ferraguti F., Cobden P., Pollard M., Cope D., Shigemoto R., Watanabe M., and Somogyi P. Immunolocalization of metabotropic glutamate receptor 1α (mGluR1α) in distinct classes of interneuron in the CA1 region of the rat hippocampus. Hippocampus 14 (2004) 193-215
17. Freund T.F., and Buzsaki G. Interneurons of the hippocampus. Hippocampus 6 (1996) 347-470
18. Gerdeman G.L., Ronesi J., and Lovinger D.M. Postsynaptic endocannabinoid release is critical to long-term depression in the striatum. Nat. Neurosci. 5 (2002) 446-451
19. Gulyas A.I., Toth K., McBain C.J., and Freund T.F. Stratum radiatum giant cells: a type of principal cell in the rat hippocampus. Eur. J. Neurosci. 10 (1998) 3813-3822
20. Hajos N., and Freund T.F. Pharmacological separation of cannabinoid sensitive receptors on hippocampal excitatory and inhibitory fibers. Neuropharmacology 43 (2002) 503-510
21. Holzer P. Local effector functions of capsaicin-sensitive sensory nerve endings: involvement of tachykinins, calcitonin gene-related peptide and other neuropeptides. Neuroscience 24 (1988) 739-768
22. Huang S.M., Bisogno T., Trevisani M., Al-Hayani A., De Petrocellis L., Fezza F., Tognetto M., Petros T.J., Krey J.F., Chu C.J., et al. An endogenous capsaicin-like substance with high potency at recombinant and native vanilloid VR1 receptors. Proc. Natl. Acad. Sci. USA 99 (2002) 8400-8405
23. Hwang S.W., Cho H., Kwak J., Lee S.Y., Kang C.J., Jung J., Cho S., Min K.H., Suh Y.G., Kim D., et al. Direct activation of capsaicin receptors by products of lipoxygenases: endogenous capsaicin-like substances. Proc. Natl. Acad. Sci. USA 97 (2000) 6155-6160
24. Jordt S.E., and Julius D. Molecular basis for species-specific sensitivity to "hot" chili peppers. Cell 108 (2002) 421-430
25. 2+-mediated mitochondrial damage and cytochrome c release. J. Immunol. 177 (2006) 4322-4329
26. Kreitzer A.C., and Regehr W.G. Retrograde inhibition of presynaptic calcium influx by endogenous cannabinoids at excitatory synapses onto Purkinje cells. Neuron 29 (2001) 717-727
27. Kreitzer A.C., and Malenka R.C. Dopamine modulation of state-dependent endocannabinoid release and long-term depression in the striatum. J. Neurosci. 25 (2005) 10537-10545
28. Kullmann D.M., and Lamsa K.P. Long-term synaptic plasticity in hippocampal interneurons. Nat. Rev. Neurosci. 8 (2007) 687-699
29. Lei S., and McBain C.J. Two loci of expression for long-term depression at hippocampal mossy fiber-interneuron synapses. J. Neurosci. 24 (2004) 2112-2121
30. Lipski J., Park T.I., Li D., Lee S.C., Trevarton A.J., Chung K.K., Freestone P.S., and Bai J.Z. Involvement of TRP-like channels in the acute ischemic response of hippocampal CA1 neurons in brain slices. Brain Res. 1077 (2006) 187-199
31. Llano I., Leresche N., and Marty A. Calcium entry increases the sensitivity of cerebellar Purkinje cells to applied GABA and decreases inhibitory synaptic currents. Neuron 6 (1991) 565-574
32. Maejima T., Hashimoto K., Yoshida T., Aiba A., and Kano M. Presynaptic inhibition caused by retrograde signal from metabotropic glutamate to cannabinoid receptors. Neuron 31 (2001) 463-475
33. Malenka R.C., and Bear M.F. LTP and LTD: an embarrassment of riches. Neuron 44 (2004) 5-21
34. Malinow R., and Tsien R.W. Presynaptic enhancement shown by whole-cell recordings of long-term potentiation in hippocampal slices. Nature 346 (1990) 177-180
35. Manabe T., Renner P., and Nicoll R.A. Postsynaptic contribution to long-term potentiation revealed by the analysis of miniature synaptic currents. Nature 355 (1992) 50-55
36. Mann E.O., and Paulsen O. Role of GABAergic inhibition in hippocampal network oscillations. Trends Neurosci. 30 (2007) 343-349
37. Marinelli S., Di Marzo V., Berretta N., Matias I., Maccarrone M., Bernardi G., and Mercuri N.B. Presynaptic facilitation of glutamatergic synapses to dopaminergic neurons of the rat substantia nigra by endogenous stimulation of vanilloid receptors. J. Neurosci. 23 (2003) 3136-3144
38. Marinelli S., Di Marzo V., Florenzano F., Fezza F., Viscomi M.T., van der Stelt M., Bernardi G., Molinari M., Maccarrone M., and Mercuri N.B. N-arachidonoyl-dopamine tunes synaptic transmission onto dopaminergic neurons by activating both cannabinoid and vanilloid receptors. Neuropsychopharmacology 32 (2007) 298-308
39. Marsch R., Foeller E., Rammes G., Bunck M., Kossl M., Holsboer F., Zieglgansberger W., Landgraf R., Lutz B., and Wotjak C.T. Reduced anxiety, conditioned fear, and hippocampal long-term potentiation in transient receptor potential vanilloid type 1 receptor-deficient mice. J. Neurosci. 27 (2007) 832-839
40. Matta J.A., Miyares R.L., and Ahern G.P. TRPV1 is a novel target for omega-3 polyunsaturated fatty acids. J. Physiol. 578 (2007) 397-411
41. McMahon L.L., and Kauer J.A. Hippocampal interneurons express a novel form of synaptic plasticity. Neuron 18 (1997) 295-305
42. Mezey E., Toth Z.E., Cortright D.N., Arzubi M.K., Krause J.E., Elde R., Guo A., Blumberg P.M., and Szallasi A. Distribution of mRNA for vanilloid receptor subtype 1 (VR1), and VR1-like immunoreactivity, in the central nervous system of the rat and human. Proc. Natl. Acad. Sci. USA 97 (2000) 3655-3660
43. Ohno-Shosaku T., Maejima T., and Kano M. Endogenous cannabinoids mediate retrograde signals from depolarized postsynaptic neurons to presynaptic terminals. Neuron 29 (2001) 729-738
44. O'Sullivan S.E., Kendall D.A., and Randall M.D. Characterisation of the vasorelaxant properties of the novel endocannabinoid N-arachidonoyl-dopamine (NADA). Br. J. Pharmacol. 141 (2004) 803-812
45. Padwal R.S., and Majumdar S.R. Drug treatments for obesity: orlistat, sibutramine, and rimonabant. Lancet 369 (2007) 71-77
46. Parra P., Gulyas A.I., and Miles R. How many subtypes of inhibitory cells in the hippocampus?. Neuron 20 (1998) 983-993
47. Pegorini S., Zani A., Braida D., Guerini-Rocco C., and Sala M. Vanilloid VR1 receptor is involved in rimonabant-induced neuroprotection. Br. J. Pharmacol. 147 (2006) 552-559
48. Pitler T.A., and Alger B.E. Postsynaptic spike firing reduces synaptic GABAA responses in hippocampal pyramidal cells. J. Neurosci. 12 (1992) 4122-4132
49. Robbe D., Kopf M., Remaury A., Bockaert J., and Manzoni O.J. Endogenous cannabinoids mediate long-term synaptic depression in the nucleus accumbens. Proc. Natl. Acad. Sci. USA 99 (2002) 8384-8388
50. 3H]resiniferatoxin autoradiography in the CNS of wild-type and TRPV1 null mice defines TRPV1 (VR-1) protein distribution. Brain Res. 995 (2004) 176-183
51. Ronesi J., Gerdeman G.L., and Lovinger D.M. Disruption of endocannabinoid release and striatal long-term depression by postsynaptic blockade of endocannabinoid membrane transport. J. Neurosci. 24 (2004) 1673-1679
52. Sanchez J.F., Krause J.E., and Cortright D.N. The distribution and regulation of vanilloid receptor VR1 and VR1 5′ splice variant RNA expression in rat. Neuroscience 107 (2001) 373-381
53. Sasamura T., Sasaki M., Tohda C., and Kuraishi Y. Existence of capsaicin-sensitive glutamatergic terminals in rat hypothalamus. Neuroreport 9 (1998) 2045-2048
54. Shibasaki K., Suzuki M., Mizuno A., and Tominaga M. Effects of body temperature on neural activity in the hippocampus: regulation of resting membrane potentials by transient receptor potential vanilloid 4. J. Neurosci. 27 (2007) 1566-1575
55. Shin J., Cho H., Hwang S.W., Jung J., Shin C.Y., Lee S.Y., Kim S.H., Lee M.G., Choi Y.H., Kim J., et al. Bradykinin-12-lipoxygenase-VR1 signaling pathway for inflammatory hyperalgesia. Proc. Natl. Acad. Sci. USA 99 (2002) 10150-10155
56. Singla S., Kreitzer A.C., and Malenka R.C. Mechanisms for synapse specificity during striatal long-term depression. J. Neurosci. 27 (2007) 5260-5264
57. Sjostrom P.J., Turrigiano G.G., and Nelson S.B. Neocortical LTD via coincident activation of presynaptic NMDA and cannabinoid receptors. Neuron 39 (2003) 641-654
58. Smart D., Gunthorpe M.J., Jerman J.C., Nasir S., Gray J., Muir A.I., Chambers J.K., Randall A.D., and Davis J.B. The endogenous lipid anandamide is a full agonist at the human vanilloid receptor (hVR1). Br. J. Pharmacol. 129 (2000) 227-230
59. + currents by muscarinic and metabotropic glutamate receptors in immature rat hippocampus. J. Physiol. 580 (2007) 411-422
60. Steenland H.W., Ko S.W., Wu L.J., and Zhuo M. Hot receptors in the brain. Mol. Pain 2 (2006) 34
61. Szabo T., Biro T., Gonzalez A.F., Palkovits M., and Blumberg P.M. Pharmacological characterization of vanilloid receptor located in the brain. Brain Res. Mol. Brain Res. 98 (2002) 51-57
62. Szallasi A., and Blumberg P.M. Vanilloid (capsaicin) receptors and mechanisms. Pharmacol. Rev. 51 (1999) 159-212
63. Szallasi A., and Appendino G. Vanilloid receptor TRPV1 antagonists as the next generation of painkillers. Are we putting the cart before the horse?. J. Med. Chem. 47 (2004) 2717-2723
64. Szallasi A., Cruz F., and Geppetti P. TRPV1: a therapeutic target for novel analgesic drugs?. Trends Mol. Med. 12 (2006) 545-554
65. Takahashi K.A., and Castillo P.E. The CB1 cannabinoid receptor mediates glutamatergic synaptic suppression in the hippocampus. Neuroscience 139 (2006) 795-802
66. Tominaga M., Caterina M.J., Malmberg A.B., Rosen T.A., Gilbert H., Skinner K., Raumann B.E., Basbaum A.I., and Julius D. The cloned capsaicin receptor integrates multiple pain-producing stimuli. Neuron 21 (1998) 531-543
67. Toth A., Boczan J., Kedei N., Lizanecz E., Bagi Z., Papp Z., Edes I., Csiba L., and Blumberg P.M. Expression and distribution of vanilloid receptor 1 (TRPV1) in the adult rat brain. Brain Res. Mol. Brain Res. 135 (2005) 162-168
68. Tucci S.A., Halford J.C., Harrold J.A., and Kirkham T.C. Therapeutic potential of targeting the endocannabinoids: implications for the treatment of obesity, metabolic syndrome, drug abuse and smoking cessation. Curr. Med. Chem. 13 (2006) 2669-2680
69. Van Der Stelt M., and Di Marzo V. Endovanilloids. Putative endogenous ligands of transient receptor potential vanilloid 1 channels. Eur. J. Biochem. 271 (2004) 1827-1834
70. Vellani V., Mapplebeck S., Moriondo A., Davis J.B., and McNaughton P.A. Protein kinase C activation potentiates gating of the vanilloid receptor VR1 by capsaicin, protons, heat and anandamide. J. Physiol. 534 (2001) 813-825
71. Wilson R.I., and Nicoll R.A. Endogenous cannabinoids mediate retrograde signalling at hippocampal synapses. Nature 410 (2001) 588-592
72. Wu Z.Z., Chen S.R., and Pan H.L. Transient receptor potential vanilloid type 1 activation down-regulates voltage-gated calcium channels through calcium-dependent calcineurin in sensory neurons. J. Biol. Chem. 280 (2005) 18142-18151
73. 2+ channels by transient receptor potential vanilloid type 1 stimulation with olvanil in primary sensory neurons. Neuroscience 141 (2006) 407-419
74. Zygmunt P.M., Petersson J., Andersson D.A., Chuang H., Sorgard M., Di Marzo V., Julius D., and Hogestatt E.D. Vanilloid receptors on sensory nerves mediate the vasodilator action of anandamide. Nature 400 (1999) 452-457